Intracellular Redox Compartmentation and ROS-Related Communication in Regulation and Signaling

Recent years have witnessed enormous progress in understanding redox signaling related to reactive oxygen species (ROS) in plants. The consensus view is that such signaling is intrinsic to many developmental processes and responses to the environment. ROS-related redox signaling is tightly wedded to compartmentation. Because membranes function as barriers, highly redox-active powerhouses such as chloroplasts, peroxisomes, and mitochondria may elicit specific signaling responses. However, transporter functions allow membranes also to act as bridges between compartments, and so regulated capacity to transmit redox changes across membranes influences the outcome of triggers produced at different locations. As well as ROS and other oxidizing species, antioxidants are key players that determine the extent of ROS accumulation at different sites and that may themselves act as signal transmitters. Like ROS, antioxidants can be transported across membranes. In addition, the intracellular distribution of antioxidative enzymes may be modulated to regulate or facilitate redox signaling appropriate to the conditions. Finally, there is substantial plasticity in organellar shape, with extensions such as stromules, peroxules, and matrixules playing potentially crucial roles in organelle-organelle communication. We provide an overview of the advances in subcellular compartmentation, identifying the gaps in our knowledge and discussing future developments in the area

Nature’s pulse power: legumes, food security and climate change

Global food security requires a major re-focusing of plant sciences, crop improvement and production agronomy towards grain legumes (pulse crops) over coming decades, with intensive research and development to identify climate-resilient species and cultivars with improved grain characteristics. Labs contributing to this special issue have undertaken research and breeding to improve pulse crops, together with innovative production agronomy which contributes to the sustainability of cropping systems. The reviews and research together form an invaluable resource for the research community and policymakers

Inhibitor-induced oxidation of the nucleus and cytosol in Arabidopsis thaliana: implications for organelle to nucleus retrograde signalling

Concepts of organelle-to-nucleus signalling pathways are largely based on genetic screens involving inhibitors of chloroplast and mitochondrial functions such as norflurazon, lincomycin (LINC), antimycin A (ANT) and salicylhydroxamic acid. These inhibitors favour enhanced cellular oxidation, but their precise effects on the cellular redox state are unknown. Using the in vivo reduction–oxidation (redox) reporter, roGFP2, inhibitor-induced changes in the glutathione redox potentials of the nuclei and cytosol were measured in Arabidopsis thaliana root, epidermal and stomatal guard cells, together with the expression of nuclear-encoded chloroplast and mitochondrial marker genes. All the chloroplast and mitochondrial inhibitors increased the degree of oxidation in the nuclei and cytosol. However, inhibitor-induced oxidation was less marked in stomatal guard cells than in epidermal or root cells. Moreover, LINC and ANT caused a greater oxidation of guard cell nuclei than the cytosol. Chloroplast and mitochondrial inhibitors significantly decreased the abundance of LHCA1 and LHCB1 transcripts. The levels of WHY1, WHY3 and LEA5 transcripts were increased in the presence of inhibitors. Chloroplast inhibitors decreased AOXA1 mRNA levels, while mitochondrial inhibitors had the opposite effect. Inhibitors that are used to characterize retrograde signalling pathways therefore have similar general effects on cellular redox state and gene expression

Photosynthesis solutions to enhance productivity

The concept that photosynthesis is a highly inefficient process in terms of conversion of light energy into biomass is embedded in the literature. It is only in the past decade that the processes limiting photosynthetic efficiency have been understood to an extent that allows a step change in our ability to manipulate light energy assimilation into carbon gain. We can therefore envisage that future increases in the grain yield potential of our major crops may depend largely on increasing the efficiency of photosynthesis. The papers in this issue provide new insights into the nature of current limitations on photosynthesis and identify new targets that can be used for crop improvement, together with information on the impacts of a changing environment on the productivity of photosynthesis on land and in our oceans. This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’

Reactive oxygen species, oxidative signaling and the regulation of photosynthesis

Reduction-oxidation (redox) reactions, in which electrons move from a donor to an acceptor, are the functional heart of photosynthesis. It is not surprising therefore that reactive oxygen species (ROS) are generated in abundance by photosynthesis, providing a plethora of redox signals as well as functioning as essential regulators of energy and metabolic fluxes. Chloroplasts are equipped with an elaborate and multifaceted protective network that allows photosynthesis to function with high productivity even in resource-limited natural environments. This includes numerous antioxidants with overlapping functions that provide enormous flexibility in redox control. ROS are an integral part of the repertoire of chloroplast signals that are transferred to the nucleus to convey essential information concerning redox pressure within the electron transport chain. Current evidence suggests that there is specificity in the gene-expression profiles triggered by the different ROS signals, so that singlet oxygen triggers programs related to over excitation of photosystem (PS) II while superoxide and hydrogen peroxide promote the expression of other suites of genes that may serve to alleviate electron pressure on the reducing side of PSI. Not all chloroplasts are equal in their signaling functions, with some sub-populations appearing to have better contacts/access to the nucleus than others to promote genetic and epigenetic responses. While the concept that light-induced increases in ROS result in damage to PSII and photoinhibition is embedded in the photosynthesis literature, there is little consensus concerning the extent to which such oxidative damage happens in nature. Slowly reversible decreases in photosynthetic capacity are not necessarily the result of light-induced damage to PSII reaction centers

Cross-tolerance to biotic and abiotic stresses in plants: a focus on resistance to aphid infestation

Plants co-evolved with an enormous variety of microbial pathogens and insect herbivores under daily and seasonal variations in abiotic environmental conditions. Hence, plant cells display a high capacity to respond to diverse stresses through a flexible and finely balanced response network that involves components such as reduction-oxidation (redox) signalling pathways, stress hormones and growth regulators, as well as calcium and protein kinase cascades. Biotic and abiotic stress responses use common signals, pathways and triggers leading to cross tolerance phenomena, whereby exposure to one type of stress can activate plant responses that facilitate tolerance to several different types of stress. While the acclimation mechanisms and adaptive responses that facilitate responses to single biotic and abiotic stresses have been extensively characterised, relatively little information is available on the dynamic aspects of combined biotic/abiotic stress response. In this review, we consider how the abiotic environment influences plant responses to attack by phloem-feeding aphids. Unravelling the signalling cascades that underpin cross tolerance to biotic and abiotic stresses will allow the identification of new targets for increasing environmental resilience in crops

Glutathione – linking cell proliferation to oxidative stress

Significance: The multifaceted functions of reduced glutathione (gamma-glutamyl-cysteinyl-glycine; GSH) continue to fascinate plants and animal scientists, not least because of the dynamic relationships between GSH and reactive oxygen species (ROS) that underpin reduction/oxidation (redox) regulation and signalling. Here we consider the respective roles of ROS and GSH in the regulation of plant growth, with a particular focus on regulation of the plant cell cycle. Glutathione is discussed not only as a crucial low molecular weight redox buffer that shields nuclear processes against oxidative challenge but also a flexible regulator of genetic and epigenetic functions. Recent Advances: The intracellular compartmentalization of GSH during the cell cycle is remarkably consistent in plants and animals. Moreover, measurements of in vivo glutathione redox potentials reveal that the cellular environment is much more reducing than predicted from GSH/GSSG ratios measured in tissue extracts. The redox potential of the cytosol and nuclei of non-dividing plant cells is about -300 mV. This relatively low redox potential is maintained even in cells experiencing oxidative stress by a number of mechanisms including vacuolar sequestration of GSSG. We propose that regulated ROS production linked to glutathione-mediated signalling events are the hallmark of viable cells within a changing and challenging environment. Critical Issues: The concept that the cell cycle in animals is subject to redox controls is well established but little is known about how ROS and GSH regulate this process in plants. However, it is increasingly likely that similar redox controls exist in plants, although possibly through different pathways. Moreover, redox-regulated proteins that function in cell cycle checkpoints remain to be identified in plants. While GSH-responsive genes have now been identified, the mechanisms that mediate and regulate protein glutathionylation in plants remain poorly defined. Future Directions: The nuclear GSH pool provides an appropriate redox environment for essential nuclear functions. Future work will function on how this essential thiol interacts with the nuclear thioredoxin system and nitric oxide to regulate genetic and epigenetic mechanisms. The characterization of redox-regulated cell cycle proteins in plants, and the elucidation of mechanisms that facilitate GSH accumulation in the nucleus are keep steps to unravelling the complexities of nuclear redox controls

Nitrate, NO and ROS Signaling in Stem Cell Homeostasis

Shoot and root growth is facilitated by stem cells in the shoot and root apical meristems (SAM and RAM). Recent reports have demonstrated a close link between nitrogen nutrition, nitric oxide (NO), and reactive oxygen species (ROS) in the regulation of SAM and RAM functions in response to nitrogen availability